Chemical Modification of Influenza CD8+ T-Cell Epitopes Enhances Their Immunogenicity Regardless of Immunodominance

PLoS One. 2016 Jun 22;11(6):e0156462. doi: 10.1371/journal.pone.0156462. eCollection 2016.

Abstract

T cells are essential players in the defense against infection. By targeting the MHC class I antigen-presenting pathway with peptide-based vaccines, antigen-specific T cells can be induced. However, low immunogenicity of peptides poses a challenge. Here, we set out to increase immunogenicity of influenza-specific CD8+ T cell epitopes. By substituting amino acids in wild type sequences with non-proteogenic amino acids, affinity for MHC can be increased, which may ultimately enhance cytotoxic CD8+ T cell responses. Since preventive vaccines against viruses should induce a broad immune response, we used this method to optimize influenza-specific epitopes of varying dominance. For this purpose, HLA-A*0201 epitopes GILGFVFTL, FMYSDFHFI and NMLSTVLGV were selected in order of decreasing MHC-affinity and dominance. For all epitopes, we designed chemically enhanced altered peptide ligands (CPLs) that exhibited greater binding affinity than their WT counterparts; even binding scores of the high affinity GILGFVFTL epitope could be improved. When HLA-A*0201 transgenic mice were vaccinated with selected CPLs, at least 2 out of 4 CPLs of each epitope showed an increase in IFN-γ responses of splenocytes. Moreover, modification of the low affinity epitope NMLSTVLGV led to an increase in the number of mice that responded. By optimizing three additional influenza epitopes specific for HLA-A*0301, we show that this strategy can be extended to other alleles. Thus, enhancing binding affinity of peptides provides a valuable tool to improve the immunogenicity and range of preventive T cell-targeted peptide vaccines.

MeSH terms

  • Amino Acid Sequence
  • Amino Acids / chemistry
  • Animals
  • CD8-Positive T-Lymphocytes / immunology*
  • Epitopes, T-Lymphocyte / chemistry
  • Epitopes, T-Lymphocyte / immunology*
  • Flow Cytometry
  • Fluorescence Polarization
  • HLA-A2 Antigen / immunology
  • HLA-A3 Antigen / immunology
  • Humans
  • Immunodominant Epitopes / chemistry
  • Immunodominant Epitopes / immunology*
  • Influenza, Human / immunology*
  • Lymphocyte Activation / immunology
  • Mice, Transgenic
  • Orthomyxoviridae Infections / immunology
  • Peptides / chemistry
  • Protein Binding
  • Vaccination

Substances

  • Amino Acids
  • Epitopes, T-Lymphocyte
  • HLA-A*02:01 antigen
  • HLA-A*03:01 antigen
  • HLA-A2 Antigen
  • HLA-A3 Antigen
  • Immunodominant Epitopes
  • Peptides

Grants and funding

This project was funded by the Center for Translational Molecular Medicine (CTMM) under grant Ampvacs (Contractnumber 2010016 and project number 041-301). URL for CTMM: www.ctmm.nl. This work was supported by the Institute for Chemical Immunology, an NWO Gravitation project funded by the Ministry of Education, Culture and Science of the government of the Netherlands under number ICI-00002. URL to website nwo: www.nwo.nl. Authors who received funding: SRH, JvB, JdJ, JL, HO. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.